Structure and composition of altered riparian forests in an agricultural Amazonian landscape

14 Pages·2015·0.64 MB·English

EcologicalApplications,25(6),2015,pp.1725–1738
(cid:2)2015bytheEcologicalSocietyofAmerica
Structure and composition of altered riparian forests
in an agricultural Amazonian landscape
R. CHELSEANAGY,1,2,6 STEPHENPORDER,1CHRISTOPHERNEILL,1,2 PAULOBRANDO,3,4 RAIMUNDOMOTAQUINTINO,5
ANDSEBASTIAˆOAVIZDONASCIMENTO5
1DepartmentofEcologyandEvolutionaryBiology,BrownUniversity,Providence,RhodeIsland02912USA
2EcosystemsCenter,MarineBiologicalLaboratory,WoodsHole,Massachusetts02543USA
3InstitutodePesquisaAmbientaldaAmazoˆnia(IPAM),Brası´lia-DF71503505Brazil
4DepartmentofGlobalEcology,CarnegieInstitutionforScience,Stanford,California94305-4101USA
5InstitutodePesquisaAmbientaldaAmazoˆnia(IPAM),Canarana-MT78640000Brazil
Abstract. Deforestationandfragmentationinfluencethemicroclimate,vegetationstructure,
andcompositionofremainingpatchesoftropicalforest.InthesouthernAmazon,atthefrontier
ofcroplandexpansion, forestsareconvertedandfragmentedinapatternthatleaves standing
riparianforestswhosedimensionsaremandatedbytheBrazilianNationalForestCode.These
alteredriparianforestssharemanycharacteristicsofwell-studieduplandforestfragments,but
differbecausetheyremainconnectedtolargerareasofforestdownstream,andbecausetheymay
experiencewettersoilconditionsbecausereductionofforestcoverinthesurroundingwatershed
raises groundwater levels and increases stream runoff. We compared forest regeneration,
structure,composition,anddiversityinfourareasofintactriparianforestandfourareaseachof
narrow,medium,andwidealteredriparianforeststhathavebeensurroundedbyagriculturesince
theearly1980s.Wefoundthatseedlingabundancewasreducedbyasmuchas64%andsapling
abundancewasreducedbyasmuchas67%inalteredcomparedtointactriparianforests.The
most pronounceddifferences between altered andintact forestoccurrednear forestedges and
within the narrowest sections of altered riparian forests. Woody plant species composition
differedanddiversitywasreducedinalteredforestscomparedtointactriparianforests.However,
despitebeingfragmentedforseveraldecades,largewoodyplantbiomassandcarbonstorage,the
numberofliveordeadlargewoodyplants,mortalityrates,andthesizedistributionofwoody
plantsdidnotdiffersignificantlybetweenalteredandintactriparianforests.Thus,eveninthese
relatively narrow forests with high edge:area ratios, we saw no evidence of the increases in
mortalityanddeclinesinbiomassthathavebeenfoundinothertropicalforestfragmentstudies.
However, because of the changes in both species community and reduced regeneration, it is
unclear how long this relative lack of change will be sustained. Additionally, Brazil recently
passedalawintheirNationalForestCodeallowingnarrowerriparianbuffersthanthosestudied
hereinrestoredareas,whichcouldaffecttheirlong-termsustainability.
Key words: agriculture; Amazon; Brazil; composition; diversity; forest structure; fragmentation;
riparianecosystems.
INTRODUCTION tez-Malvido1998,Lauranceetal.1998,2002,Gasconet
al.2000,OosterhoornandKappelle2000,Guariguataet
Deforestationoftropicalforestsforagricultureisoneof
al.2002,Higuchietal.2008).
themajorforcesshapingtheEarth’ssurface(Lambinetal.
Comparedtointactforests,forestfragmentsinupland
2003,LambinandMeyfroidt2011).Inadditiontodirect
lossofforestcover,landconversionfragmentsremaining areas often exhibit greater mortality of canopy and
forestbycreatingisolatedforestpatchesandforestedges emergent trees (Kapos 1989, Williams-Linera 1990,
throughout landscapes (Fearnside 2005, DeFries et al. Oosterhoorn and Kappelle 2000, Laurance et al. 2002),
2008,Nepstadetal.2008,Asneretal.2010).Uncertainty inhibition of seedling and sapling regeneration at forest
regardingtheabilityofforestfragmentstopersistinthe edges (Benitez-Malvido 1998, Gascon et al. 2000), and
landscape and provide ecosystem services has led to a increased abundance of lianas and disturbance-adapted,
numberofstudiesonfragmentationandedgeeffectsinthe light-demanding,andabioticallydispersedtreesnearthe
Neotropics, from lowland evergreen forests of Brazil to forest edges (Oliveira-Filho et al. 1997, Laurance et al.
montane cloud forests of Costa Rica (Kapos 1989, 1998, 2002, 2006, Oosterhoorn and Kappelle 2000).
Williams-Linera 1990, Oliveira-Filho et al. 1997, Beni- Reduced regeneration and increased mortality of native
vegetationintropicalforestfragmentsmaybecausedbya
combination of microclimate changes such as increased
Manuscript received 10 September 2014; revised 7 January
air temperature, reduced humidity, and greater wind
2015;accepted12January2015.CorrespondingEditor:Y.Pan.
6E-mail:[email protected] damageandlightexposure,orbychangestofireregimes,
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1726 R.CHELSEANAGYETAL. EcologicalApplications
Vol.25,No.6
which may reduce fragment areas over time from the muchofBrazil (Lima andGascon 1999,Leesand Peres
edges inward (Gascon et al. 2000, Laurance et al. 2002, 2008, Macedo et al. 2013). This is because the Brazilian
D’Angeloetal.2004).Fragmentationmayresultinlosses Forest Code mandates that land clearing practices leave
ofcarbon(C)storedinbiomassbecauseofhigherratesof standingatleast30mofforestonbothsidesofstreams
tree mortalitycoupledwithchangesinplant community lessthan10mwideto‘‘conservehydrologicalfunctions,
composition, especially when lianas and pioneer species prevent soil erosion, support frontier defence, guarantee
with low wood density replace slow-growing old-growth publichealth,protectsitesofnaturalbeautyandprovide
treeswithhighwooddensity(Lauranceetal.2002,2006, protection for rare native species of flora and fauna’’
2007), leading to more flammable fuel (Brando et al. (Stickleretal.2013).TheBrazilianstateofMatoGrosso
2012). Tree species diversity is often reduced in upland has one of the world’s highest rates of deforestation
forestfragments(TurnerandCorlett1996,Turner1996, (DeFries et al. 2008) and is now the Amazon’s biggest
Terborghetal.2001,Lauranceetal.2002),yetsomeforest and fastest-growing agricultural frontier (Brando et al.
fragments isolated more than 100 years ago in the 2013).MostofthelandinMatoGrossocurrentlybeing
Brazilian Atlantic Forest still maintain high species used for agriculture was cleared first for pasture in the
diversity(Higuchietal.2008).Thedegreeorintensityof 1980s and converted to intensive soybean (Glycine max)
past disturbance (Oliveira-Filho et al. 1997) and the cultivationafter2000(Brandoetal.2013,Galfordetal.
physicalarrangement,particularlytheedge:arearatio,of 2013,Macedoetal.2013).Thetotalareainmechanized
forestfragments(Kaposetal.1993,Lauranceetal.1998, agricultureinMatoGrossoalmostdoubledinthedecade
Chambersetal.2007)canhaveanimportantinfluenceon from 2001 to 2011, growing from 38850 to 69421 km2
theextentofalterationofforestproperties.Additionally, (VanWey et al. 2013). Understanding the ability of
somefragments andforestedges haveshown decreasing altered riparian forests to provide ecosystem services in
fragmentation and edge effects over time as vegetation thisagriculturallandscapewillbeincreasinglyimportant
regrew and the forest edge filled in (Oliveira-Filho et al. asthesepatternsoflandconversioncontinue.
1997, Didham and Lawton 1999, Laurance et al. 2002), The altered riparian forests of the southern Amazon
the presence of pioneer and light-demanding species may experience similar microclimatic shifts to those in
decreasedovertime(Higuchietal.2008),andrecruitment fragments of upland tropical forests, but they differ in
exceeded mortality, suggesting recovery in very old severalotherwaysthatmaybeimportantdeterminantsof
fragments(Oliveira-Filhoetal.1997). forestdynamics.Theyarelong,thinstripssurroundedon
Insometropicallandscapes,forestfragmentsalsoexist threesidesbyclearedlandbutconnectedtolargerareasof
as patches of forest left along stream channels. Increas- intact forest further downstream. In addition, lower
inglyimportantinareasofcroplandexpansion,theseare evapotranspiration in cropland results in more water
in some cases mandated by land-use regulations. Com- reaching riparian zones and small stream channels in
pared to forest fragments in upland regions, we know agriculturalwatersheds(Brownetal.2005,Gordonetal.
much less about the dynamics of these altered riparian 2008, Hayhoe et al. 2011, Neill et al. 2013). This may
forests. Because the latter are typically thin strips with influencegroundwaterandsoilmoistureconditionsboth
high edge:area ratios, changes to both forest microcli- in the riparian forest and in adjacent agricultural fields.
mateandtreespeciescompositionanddynamicsmaybe Therefore,trees inthesealteredriparianareasmay have
pronounced, and they are often highly altered and greater accesstosoilwater,whichcouldcompensatefor
degraded(Capon etal. 2013,Strombergetal. 2013). As greater water losses through transpiration caused by
theconfigurationandsizeofafragmentcaninfluencethe hotteranddrierairconditions,andincreasefireresistance.
degree of change following fragmentation, the width of Alternatively, this higher water table could cause addi-
theriparianbufferleftbehindinalteredlandscapes may tional stress if the roots are inundated for long time
similarly influence changes in forest structure and periods.Itisalsopossiblethatalteredriparianforestsin
composition. However, there is some evidence that agriculturallandscapesareresistanttochangeandsimilar
riparian ecosystems may be more resilient than other insomewaystostreamsideorgalleryforeststhatexistas
systems because of their inherently heterogeneous envi- natural fragments in drier landscapes, although the
ronmental conditions, which include alternating periods mechanismofisolationandtimesinceisolationcertainly
of wet and dry conditions. Understanding the fate of differ. Studies in Belize and Venezuela indicated that
tropical riparian forests in increasingly fragmented galleryforestscontainhightreespeciesdensitiesandrates
landscapes is important because these forests are highly oftreegrowthandturnoversimilartothoseincontinuous
valuedforprovidingcriticalecosystemservices,including forests (Meave et al. 1991, MacDougall and Kellman
refugia for plant and animal species in aquatic, semi- 1992,Kellmanetal.1998).
aquatic, and terrestrial areas, and protecting stream We studied riparian forests in the Brazilian state of
resourcesbymaintainingstreamtemperatureandreduc- Mato Grosso in the southern Amazon to see if they
ingerosionofsedimentsandnutrients(Meaveetal.1991, respond similarly to upland forest fragments or natu-
Naimanetal.2005,Malhietal.2008). rally isolated gallery forests because they share charac-
Altered riparian forests are now common in agricul- teristics with both. We compared riparian forests
turallandscapesofthesouthernAmazonandthroughout surrounded by agricultural cropland with riparian
September2015 ISOLATIONOFAMAZONIANRIPARIANFORESTS 1727
FIG.1. MapoftheFazendaTangurofarmboundaries(MatoGrosso,Brazil)withaltered(surroundedbysoybeans;Glycine
max)andintact(surroundedbyforest)riparianforesttransectlocations.ThebackgroundimageisaLandsat5TMfalsecolor
satelliteimage(bands5,4,and3)fromJune2011.Theinsetsshowthestudydesignofvegetationanalysisinalteredriparianforests:
plots(5310 m; for trees) andsubplotswithin the plots(131 m; for herbaceouscover). Intactriparian forestswere sampled
similarly,withtransectlengthsmirroringthosefoundinthemediumwidth(W2;185–210mwide)alteredriparianzones.
forests within large areas of remaining intact tropical 52823008.8500 W). The mean annual temperature is 258C
forest to examine how fragmentation of riparian forest and mean annual precipitation from 2005 to 2011 was
influences forest vegetation dynamics and ecosystem 1770mm/yr(Rochaetal.2013).Theregionexperiencesa
services including C storage and biodiversity. We distinctdryseasonfromMaytoAugust,whenrainfallis
addressed the following questions: (Question 1) Do ,10mm/month(Rochaetal.2013).Today,50%ofthe
altered riparian forests have altered microclimates, ranch remains in closed-canopy evergreen forests inter-
including hotter and drier conditions, and are changes mediate in stature between the more humid rain forests
tomicroclimategreatestnearforestedges?(Question2) tothenorthandCerrado(Braziliansavanna)vegetation
Have altered riparian forests degraded over time to the south (Ivanauskas et al. 2004, Balch et al. 2008).
through loss of large trees and biomass, reduced tree TherestoftheareaonFazendaTangurowasdeforested
regeneration, and decreased species richness? (Question for pasture in the early 1980s. During forest clearing,
3) Are changes to altered riparian forest structure some riparian buffers surrounding streams were left in
greater in narrower compared with wider forest rem- place.Impoundmentswerealsoconstructedonheadwa-
nants? (Question 4) Has increased water availability ter streams throughout the region to provide water for
causedbyahigherwatertablebufferedalteredriparian cattle (Macedo et al. 2013). To initiate soybean
forests against the microclimatic changes typically cultivation beginning in 2003, remaining woody vegeta-
associatedwithfragmentation? tion was piled into rows and burned and the soil was
Thiswork,particularlyempiricalinformationderived tilled,afterwhichsoybeanswereplantedandmaintained
from Question 3, can inform policy decisions regarding usingno-tillpractices(Riskinetal.2013).
forest management practices and mandated riparian
buffer widthin Brazil. Experimental design
We studied riparian forests along four headwater
METHODS
streamsflowingthroughsoybeanfields(alteredriparian
Site description
forests), and four streams flowing through intact forest
Fazenda Tanguro is an 800-km2 soybean farm in the (Fig. 1). We use the term ‘‘edge’’ to mean the forest
Brazilian state of Mato Grosso (13804035.3900 S, fragmentedgeadjacenttothesoybeanfield,nottheless-
1728 R.CHELSEANAGYETAL. EcologicalApplications
Vol.25,No.6
pronouncedforestedgethatexistsalongthestream.For We counted seedlings (,5 cm diameter at breast
eachofthestreamssurroundedbysoybeans,wecreated height[dbh]and,30cmheightandlargeenoughtobe
three transects perpendicular to the stream in the seenbythenakedeye),saplings(,5cmdbhand(cid:2)30cm
remaining riparian vegetation at three forest widths: height),andlianasandestimatedpercentcoverofgrass,
narrow(W1;75–90mwidefromedgetoedge),medium forbs,andfernsinfive1-m2subplotsarrayeddiagonally
(W2;185–210m),andwide(W3;210–325m).Thethree across each of the larger vegetation plots (Fig. 1). We
riparian forest widths were included to look for the measured all live and dead woody plants (including
presence of a threshold (Question 3) below or above trees, lianas, and palms) (cid:2)5 cm dbh in each 5310 m
which riparian forest properties change to inform plot (Question 2). To confirm dead vs. living trees, the
management decisions on mandated riparian widths. bark was cut and examined for water flowing in the
All three of these width classes exceed the width xylem in trees suspected to be dead. To calculate the
mandated by the Brazilian Forest Code (30 m on both biomassofeachtree,weappliedanallometricequation
sides of the stream). The altered riparian forests were from Chave et al. (2005) developed for tropical moist
asymmetrical;thedistancefromtheedgeoftheriparian forestswitha pronounceddryseason
vegetationtothestreamwasnotequalonthetwosides
lnðAGBÞ¼aþb3lnðdbhÞþlnðqÞ
of the stream. All transects in altered riparian forests
wereatleast200mdownstreamfromimpoundmentsto incorporating aboveground biomass (in kg; AGB), dbh
limittheir effectonriparianvegetation. Riparianforest (incm),andwoodspecificgravity(q;ing/cm3);aandb
plotsshowednosignofpreviousloggingasindicatedby areconstantsforatropicalmoistforestequalto(cid:3)1.864
stumps or other signs beyond the current maintenance and 2.608, respectively. We chose the wood mean
of farm-field edges. specific gravity for the site (Mato Grosso, Brazil) to be
0.61g/cm3,basedonCarvalhoetal.(2001).Tocalculate
We mirrored the design of the altered riparian forest
the aboveground biomass of each palm, we used an
transects in the intact riparian forests. We established
equationfrom Goodmanet al.(2013)
fourtransectsthatcrossedsimilar-sizedstreams(2.1–5.7
and 2.7–4.7 m wide in intact and altered forests, lnðAGBÞ¼(cid:3)3:3488þ2:74833lnðdbhÞ:
respectively) and had the same length as the transects
in the fourW2altered riparian forests. To calculate the aboveground biomass of each liana,
Along each of the 16 transects, we sampled the weused anequationfrom Gehringet al.(2004)
vegetation in six 5 3 10 m plots (300 m2/transect) to
lnðAGBÞ¼(cid:3)7:114þ2:2763lnðDÞ
characterize stream, mid-riparian zone (mid), and edge
vegetation(Fig.1).Severalsmallerplotswerechosenas where D is diameter at 30 cm height (in mm). To
opposed to one larger plot because we expected calculatethelianadiameterat30cmheight,wefollowed
variation in both vegetation (Kellman et al. 1998) and the equationfrom Gehringet al.(2004)
drivers of change (e.g., altered microclimate) within
D¼1:235dbhþ0:002dbh2:
riparian forests, with vegetation differences most pro-
nouncedatforestedges(Question1).Thisplotsizeand WecalculatedCcontentoftrees,palms,andlianasas
configuration maximized the available width of altered 50%ofthebiomassofeachwoodyplant.Wecalculated
riparianforestswhilekeepingplotsizeconsistentamong the basal area (cross-sectional area) of all large woody
sites at different riparian widths. Plot length was plantswith theequation
constricted by (1) meandering streams and riparian
(cid:2)dbh(cid:3)2
buffer vegetation that followed these contours, (2) BA¼p
maintaining a minimum distance of 200 m from each 2
of the impoundments, and (3) maintaining a minimum whereBAisthebasalarea.Were-censusedtreesoneyear
distance of 0.5 km between transects to discretize sites after initial plot establishment and calculated annual
among the three width categories. Each transect had a mortality as the number of newly dead trees per plot
complete set of the plot locations (edge, mid, and dividedbythetotalnumberoftreesperplot.Weassayed
stream) on each side of the stream (Fig. 1). Because canopy cover using leaf area index (LAI) measurements
therewasnocomparableedgeinintactriparianforests, from a LAI-2000 plant canopy analyzer (LI-COR,
theplotswerelocatedatdistancesfromthestreamsuch Lincoln,Nebraska,USA)every10malongeachtransect
thattheyreplicatedthedistancestothestream,mid,and intheintactandW2alteredriparianforestsonly.
edge in the W2 altered riparian forest transects. In We identified plants (cid:2)5 cm dbh (including trees,
additiontothecategoricalparametersofedge,mid,and palms,andlianas)tospecies,whenpossible.Thefloraof
stream, we measured the distance to the stream and the region is well known, and local botanists from the
distance to the nearest edge to use as continuous Instituto de Pesquisa Ambiental da Amazoˆnia (IPAM)
explanatory variables. The distance of each plot center identified the trees. If the species was unknown, trees
to the nearest edge (altered riparian forests only) or to were identified to the genus level. If the genus was
the stream wasmeasured inthe field. unknown, trees were included in an ‘‘unknown’’
September2015 ISOLATIONOFAMAZONIANRIPARIANFORESTS 1729
category that encompassed 41 of 862 or 4.75% of the Madrid, Spain). We used pressure data from the water
total number of trees in all plots. Unknown trees were levelloggersandconvertedittothewaterdepthbelowthe
excludedfromcompositionalanalyses,butwereinclud- soilsurface.Tomapaprofileofthewatertablefromwell
ed in structural analyses (size distribution, biomass, towellalongeachtransect,wesubtractedthedepthofthe
etc.).Toreducetheinfluenceofextremelyrarespecies,if watertablebelowthesoilsurfacefromthewell’srelative
therewasonlyonetreeofaknownspeciesfoundinany elevation(relativetothemostuplandwellinthetransect).
of the plots (i.e., singletons) we removed that species
Statistical analysis
fromthecompositionalanalyses(Totietal.2000).Asa
metric of a species’ contribution to the community, we AllstatisticalcomparisonsweredoneinRversion3.0.1
calculated the importance value index (IVI) for each (RCoreTeam2013),andweassessedsignificanceatP,
speciesateach siteusingthe following equation: 0.05.Allvariablesweretestedfornormality;ifthedatadid
not approach normality, a suite oftransformations were
IVI¼RBAþRDþRF
employed(log,squareroot,etc.)andifnormalitywasstill
where IVI is the importance value index, RBA is the notachieved,nonparametricstatisticaltestswereused.
relativebasalarea((basalareaofeachspecies/totalbasal We compared differences in temperature, relative
area of all species) 3 100), RD is the relative density humidity, VPD,and light at forestedges (0m along the
((number of individuals per species per plot/total transect)inW2alteredandintactriparianforestswitha
number of individuals of all species per plot) 3 100), Wilcoxon signed rank test. We analyzed the water table
andRFistherelativefrequency((numberofoccurrenc- depth in paired wells in intact and W2 altered riparian
es of each species/number of occurrences of all species siteswithapairedttest.
combined) 3 100)), following Dangol and Shivakoti WeusedaGtestofindependencewitharowbycolumn
(2001)andBautista et al.(2014). (R3C)contingencytabletoanalyzewhethercounts of
Wemonitoredairtemperature,relativehumidity, and seedlings and saplings differed among forest types and
locations (Sokal and Rohlf 1995). We also analyzed
light(wetseasononly)simultaneouslyalongaW2altered
counts of seedlings, saplings, lianas, and live and dead
riparian forests and its paired intact riparian forest
trees among forest types (intact riparian forest and W1,
transect using HOBO Tidbit v2 water temperature data
W2,andW3alteredriparianforests)andlocations(edge,
loggers,HOBOU23Prov2temperature/relativehumidity
mid, stream) using generalized linear models with a
dataloggers,andHOBOPendanttemperature/lightdata
PoissondistributionandHSDtests(Rpackageagricolae;
loggers (Onset, Bourne, Massachusetts, USA). We
Mendiburu 2014) when we found significant differences
collected data from three different transect pairs over
amonggroups(KindtandCoe2005).WeusedaKruskal-
thecourseofthreeweeksinthedryseason(18June–9July
Wallisranksumtesttoanalyzepercentgrasscoveramong
2013, measured every 30 min for six continuous days in
foresttypes(intact,W1,W2,W3).Weanalyzedmortality
each altered–intact pair), and for one transect pair over
among forest types and locations using Kruskal-Wallis
thecourseofoneweekintherainy season(8–14March
ranksumtests.
2013,measuredevery30min).Weplacedloggersroughly
Inadditiontoanalyzingplotsindiscretecategoriesof
every 20 m along each transect, depending on the total
location (edge, mid, stream), we compared counts of
transect length. We calculated vapor pressure deficit
seedlings, saplings, lianas, and live and dead trees in
(VPD;inPa)withthefollowingequation
altered riparian forests to the distance from the stream
(cid:2) RH(cid:3) and distance from the nearest edge using generalized
VPD¼ 1(cid:3) 3SVP
100 linearmodelswithaPoissondistribution(KindtandCoe
2005).Wecomparedmeantreedbhtothedistancefrom
where RH is the relative humidity (%) and SVP is the
the stream and distance from the nearest edge using
saturatedvaporpressure(Pa).SVPwascalculatedfrom
multipleregression.
SVP¼610:7310ð7:5T=237:3þTÞ Tocomparesizedistributionsofalltreesamongforest
types(intactvs.W1,intactvs.W2,andintactvs.W3),we
whereTisthetemperature(8C;MonteithandUnsworth usedFisher’sexacttests(Kindtand Coe2005).Wealso
1990). compared tree size distributions, with binned tree
To measure water table depth along the transects, we diameters (e.g., 5–10 cm, 10–15 cm), of all four forest
installedfourtosixwellsalongeachintactandW2altered types(intact,W1,W2,W3)simultaneouslyusingaGtest
riparianforesttransect.WeplacedHOBOU20waterlevel ofindependence(SokalandRohlf1995).
loggersinwellsofeachtransectpair(n¼threepairs)for WeanalyzedabovegroundlargewoodyplantCstocks
roughly one-weekintervalsinthedry season(18 June–9 using ANOVA on log -transformed data. We used a t
10
July2013),whenweexpectedthedifferencesinwatertable testtocompareLAIalongtransectsinintactandaltered
heightbetweenforesttypestobegreatest.Wedetermined (W2 only) riparian transects and linear regression to
the change in relative elevation along the transect using compareLAIanddistancetothenearestedge.
traditionalsurveyingmethodsusinganAT-G2automatic Foranalysisofspeciescompositionanddiversity,we
level, tripod, and surveyor’s rod (Topcon Positioning, excludedthemidlocationsofeachtransectbecausemid
1730 R.CHELSEANAGYETAL. EcologicalApplications
Vol.25,No.6
FIG.2. Vaporpressuredeficit(Pa)duringthedryseasonatforestedgesinFazendaTanguro(0malongtransect;atforestedge)
ofpairedsites:(a)intact1andaltered1,18–24June2013;(b)intact2andaltered2,3–9July2013;(c)intact3andaltered3,25
June–1July2013.
plots ranged from well-drained uplands to waterlogged Bray-Curtis distances are more appropriate for ecolog-
near-stream zones, depending on the configuration of ical data than metrics using Euclidian distances (e.g.,
theriparianforestandthelocationofthestreamwithin principal components analysis; Faith et al. 1987, Kindt
the relatively flat area on either side of the stream and Coe 2005). To make the PCoA graph, we used the
channel.Incontrast,theedgeandstreamlocationswere ggplot2(Wilson 2009)package features.
always upland or adjacent to the stream channel, To study large woody plant species diversity, we
respectively. To examine the effect of forest type and calculatedthespeciesrichness,Shannondiversityindex,
plot location on species composition, we grouped the Simpson index, and inverse Simpson index for each
two sides of each stream while keeping each stream foresttype(intact, W1,W2,W3).
separate. Thus for all analyses of species composition
RESULTS
anddiversity,weanalyzedatotalof32sites:16adjacent
to a stream, and 16 at the forest edge (or the same Microclimateandhydrology
distance from the stream in intact forest as one of the During the dry season, edges of altered riparian
edgesin the altered riparian forest). forests were significantly hotter and had significantly
To analyze species composition of all large woody lower relative humidity (RH) than edges of intact
plants with dbh (cid:2)5 cm, we selected a similarity metric, riparian forests (mean values of 22.68C vs. 21.28C and
Kulczynski distance, and the constrained ordination 92.9% RH vs. 83.8% RH for altered and intact,
method, principal coordinates analysis (PCoA) with respectively). Mean VPD was significantly higher at
Bray-Curtis distance method, in the BiodiversityR alteredriparianforestsedgesthanintactriparianforests
(KindtandCoe2005)andRcmdr(Fox2005)packages edges in the dry season (606 Pa compared to 226 Pa),
to plot differences in species abundances among sites with the greatest differences just after midday (Fig. 2).
(Kindt and Coe 2005). Both the Kulczynski and the Duringthedryseason,thewatertablewassignificantly
September2015 ISOLATIONOFAMAZONIANRIPARIANFORESTS 1731
cantly(meanvaluesof25.58Cand26.18Cforintactand
alteredriparianforestedges,respectively).Wewerenot
abletocollectRHdatafromforestedgesduringthewet
season and therefore cannot calculate VPD during this
time.Therewassignificantlymorelight(asmeasuredin
lux)attheedgesofalteredriparianforeststhanatedges
of intact riparian forests during the wet season (mean
valuesof6490lxforalteredriparianforestsand3200lx
for intact riparianforests).
Seedlings andsaplings
There were significantly fewer seedlings in narrow
(W1), medium (W2), and wide (W3) altered riparian
forests compared with intact riparian forests (Table 1).
These differences in seedling numbers were most
pronounced among edge plots (Table 2). There were
significantly fewer saplings in W1 and W2 altered
riparian forests compared with W3 altered and intact
riparianforests(Table1).Saplingsweresignificantlyless
abundant in W1 and W2 sites in both edge and stream
plots (Table 2). The number of seedlings and saplings
increased with increasing distance from the stream in
altered riparian forests (Table 3). There was no
difference in counts of seedlings and saplings across all
forest type (intact, W1, W2, W3) and location (stream,
mid,edge)simultaneouscombinations(datanotshown).
FIG.3. Meanadjustedwatertabledepth(mbelowground) Foreststructure andfunctionalcomposition
relativetothestartingtransectelevationinwellsforalteredand
LAI at forest edges (0 m along the transect) did not
intact paired sites.(a) Intact1 andaltered 1;(b) intact 2 and
altered 2; (c) intact 3 and altered 3. The light gray dashed differbetweenintactandalteredriparianforests(4.56
verticallinerepresentsthestreamlocationalongeachtransect. 0.4 for intact and 4.4 6 0.5 for [W2] altered riparian
Datashownaremeanvaluesovertheentire;1-weekintervalat forests; all means shown 6 SE), but was significantly
eachsitepairinthedryseason(18June–9July2013).
lower along entire transects in altered than intact
riparian forests (Fig. 4). There was more variation in
closertothesoilsurfaceinalteredthaninintactriparian LAI among streams in altered than in intact riparian
forests,sometimes byseveral meters (Fig.3). forests (Fig. 4). LAI was positively and significantly
Duringthewetseason,thetemperatureattheedgesof related to the distance from the nearest edge (data not
intact vs. altered riparian forests did not vary signifi- shown).
TABLE1. Descriptivestatisticsforlargewoodyplants(cid:2)5cmdiameteratbreastheight(dbh),smallplants,5cmdbh,andgrass
coveratFazendaTanguro,an800-km2soybeanfarminMatoGrosso,Brazil.
Alteredforest
Vegetationcomponent Units Intactforest W2 W3
W1
Plots
Alllargewoodyplants no./50m2 8.1a(0.7) 9.1a(0.7) 8.4a(0.6) 9.3a(0.7)
Deadwoodyplants no./50m2 0.7a(0.2) 0.8a(0.2) 0.4a(0.2) 0.6a(0.2)
Treesonly no./50m2 7.1c(0.5) 8.8ab(0.7) 8.1b(0.6) 9.0a(0.8)
Palmsonly no./50m2 0.6a(0.4)(cid:2) 0.0a(0.0)(cid:2) 0.3a(0.2)(cid:2) 0.2a(0.1)(cid:2)
Largelianas no./50m2 0.4a(0.1)(cid:2) 0.4a(0.1)(cid:2) 0.0a(0.0)(cid:2) 0.2a(0.1)(cid:2)
Subplots
Seedlings no./m2 21.2a(4.0) 12.6c(1.6) 13.1c(1.9) 15.7b(3.6)
Saplings no./m2 5.7a(0.5) 2.4b(0.2) 2.5b(0.4) 5.3a(0.8)
Smalllianas no./m2 0.8b(0.1) 1.6ab(0.4) 2.0a(0.4) 1.9a(0.4)
Grass %cover 2.8a(1.0) 6.5a(3.0) 9.4a(2.3) 8.1a(2.5)
Notes:Meansareshownwithstandarderrorinparentheses.Significantdifferencesinmeanvaluesareindicatedbydifferent
superscriptedletters.Plotswere50m2,subplotswere1m2.Foresttypeswereintactriparianforest,andnarrow(W1;75–90mwide
fromedgetoedge),medium(W2;185–210m),andwide(W3;210–325m)alteredriparianforest.
(cid:2)Asignificantdifferencewasfoundamongmeans,butpairwiseposthoccomparisonsdidnotfindadifferenceamonggroups.
1732 R.CHELSEANAGYETAL. EcologicalApplications
Vol.25,No.6
TABLE2. Numberofofseedlingsandsaplings.
Groups Intact W1 W2 W3 Devianceexplained
Seedlings
Edge 31.1a(10.7) 11.3c(1.7) 16.5b(3.7) 26.5a(9.3) 21.3%
Mid 22.0a(3.5) 15.1b(2.7) 15.0b(3.8) 13.5b(3.6) 10.8%
Stream 10.5ab(2.1) 11.9a(3.7) 8.0bc(1.6) 7.2c(1.3) 10.1%
Saplings
Edge 6.9a(3.2) 2.3b(0.3) 2.7b(0.8) 5.3a(1.1) 50%
Mid 6.1a(1.1) 2.8b(0.5) 3.2b(0.9) 5.8a(2.1) 21.3%
Stream 6.2a(0.8) 2.0b(0.2) 1.7b(0.2) 4.8a(1.1) 41.3%
Notes:Meansareshownwithstandarderrorinparentheses.Whenanalyzedamongallgroups
(foresttypeandlocation)atonce,therewerenosignificantdifferencesamonggroups.Significant
differenceswithinedge,mid,orstreamplotsonlyareindicatedbydifferentsuperscriptedletters.
Of the 862 total large woody plants (all trees, palms, altered riparian forests (Table 1). There was also a
andlianas(cid:2)5cmdbh)inallplots,63.9%wereinthe5– significant difference in the number of large lianas and
10cmdbhsizeclassandonly1.7%weregreaterthan40 palms among locations along the transect, although
cmdbh.Thesizedistributionoflargewoodyplants(Fig. pairwise comparisons did not show differences among
5) did not vary significantly among altered and intact the edge, mid, and stream groups (mean large liana
riparian forests. The number of large woody plants per counts of 0.1 6 0.1, 0.4 6 0.1, and 0.2 6 0.1 for edge,
plot did not vary significantly with forest type (intact, mid, and stream, respectively; mean palm counts of 0.0
W1, W2, W3; Table 1) or with location (edge, mid, 6 0.0, 0.4 6 0.3, and 0.4 6 0.2 for edge, mid, and
stream; data not shown). The number of dead large stream,respectively).LargewoodyplantbiomassandC
woody plants did not differ between intact and altered content did not differ significantly among forest types;
riparianforests(Table1),andamongalteredsitesonly, the mean aboveground C content was 13.2, 8.3, 15.3,
dead large woody plant abundance was not related to and 15.8 kg C/m2 for intact, W1, W2, and W3,
distance from nearest forest edge (Table 3). Annual respectively.
mortality did not vary significantly among forest types Thereweresignificantlymoresmalllianasinthewider
(3.9%61.7%,4.2%61.7%,6.5%63.4%,and2.7%6 altered riparian sites (W2 and W3) than in intact
1.1%forintact,W1,W2,andW3,respectively).Within ripariansites,butthenumberofsmalllianasinnarrow
the large woody plants, there were significantly fewer altered riparian (W1) sites did not differ significantly
treesinintactthanalteredriparianforests(Table1).The from any of the other sites (Table 1). Small liana
number of trees did not vary with location (data not abundance was significantly and negatively related to
shown). Poisson regression indicated significant differ- the distance from stream in altered riparian forests
ences in the number of large lianas and palms among (Table 3). Grass cover was low in all plots and did not
forest types, butpairwise comparisons did notallow us vary significantly among forest types (Table 1). Grass
to determine which groups differed. Numerically, large cover did vary significantly with location: grass cover
lianas were most abundant in intact and W1 and least was significantly lower in edge plots than in mid or
abundantinW2alteredriparianforests,andpalmswere stream plots (0.5% 6 0.2%, 9.7% 6 1.3%, and 9.9% 6
most abundant in intact and least abundant in W1 2.4%for edge,mid, andstream, respectively).
TABLE 3. Regressionmodelsbetweennumberoflargewoodyplants,deadwoodyplants,small
lianas, seedlings, saplings, and mean woody plant size (for woody plants (cid:2)5 cm dbh) and
distancefromstream(dst)andnearestedge(dne)foralteredriparianforestsonly.
Explanatoryvariable
Modeltypeanddependent Devianceexplained
variable First P Second P bymodel
Poisson
No.largewoodyplants dne((cid:3)) 0.83 dst 0.89 0.1%
No.deadwoodyplants dne 0.28 dst 0.77 2.0%
Meanno.smalllianas dne((cid:3)) 0.13 dst((cid:3)) ,0.001 20.8%
Meanno.seedlings dne(þ) 0.15 dst(þ) ,0.001 21.4%
Meanno.saplings dne(þ) 0.22 dst(þ) 0.001 6.5%
Multiple
log(meandbh) log(dne) 0.92 log(dst) 0.43 1.0%
Notes: Significant relationships (P , 0.05) are indicated in bold and the direction of the
relationship(þ)or((cid:3))isindicatedfollowingtheexplanatoryvariable.Thedistancetonearestedge
orstreamwasmeasuredinthefield.
September2015 ISOLATIONOFAMAZONIANRIPARIANFORESTS 1733
FIG.4. Leafareaindex(LAI;m2leafarea/m2groundarea)inintactandalteredripariansites.(a)Meanandstandarderror
acrossallintactandalteredsites(differencessignificantatP,0.05markedwithdifferentlowercaseletters),and(b)boxplotsof
LAIatindividualsites.Theboldlinewithineachboxisthemedianvalueforthatsite.Theboxendpointsarethelower(25%)and
upper(75%)quartiles,thewhiskersextendtothemostextremedatapointwhichisnomorethan1.5timestheinterquartilerange
fromthebox,andthecirclesoutsidethewhiskersareoutliers.Measurementsweretakenevery10malongthetransects.
Tree species compositionanddiversity forests shared one of the six most important species
with all altered riparian forests, two species with the
Among all plots, there were 110 known species of
W2andW3forests,andnospecieswiththeW1forests
large woody plants (trees, palms, and lianas (cid:2)5 cm
(Appendix: Table A1).
dbh). The species with the highest IVIs among all
altered riparian forests were (ranked from the most Forallwoodyplantswithdbh(cid:2)5cm,theKulczynski
important) Nectandra cuspidata, Maprounea guinanen- distance metric indicated significant differences among
sis, Tapirira guianensis, Qualea witrockii, Protium forest types (P ¼ 0.001), locations (P ¼ 0.004), and
spruceanum, and Inga heterophylla (Appendix: Table individualstreams(P¼0.001).Thefirsttwodimensions
A1).ThespecieswiththehighestIVIsinintactriparian ofthePCoAanalysisamongthe32sitesexplained44%
forests were Miconia pyrifolia, Protium guianense, ofthevarianceandseparatedtheintactriparianforests
Miconia sp., P. spruceanum, Xylopia amazonica, and fromallalteredriparianforestswithnooverlap(Fig.6).
Euterpe sp. (Appendix: Table A1). Intact riparian Species richness was highest in W2 altered riparian
FIG.5. Thenumberoflivetrees(frequency)inbinnedsizeclasses(diameteratbreastheight,dbh)inintactandnarrow(W1;
75–90mwidefromedgetoedge),medium(W2;185–210m),andwide(W3;210–325m)alteredriparianforestsplots.
1734 R.CHELSEANAGYETAL. EcologicalApplications
Vol.25,No.6
forests,butthreediversityindices,theShannondiversity forestcanopiesinforestfragmentsandnearforestedges
index, the Simpson diversity index, and the inverse (Williams-Linera 1990, Kapos et al. 1993, Laurance et
Simpsonindex,foundhigherdiversityinintactthanall al. 1998, Oosterhoorn and Kappelle 2000, Chambers et
altered riparian sites(Table 4). al.2007) wasonlyweakly supportedatoursites.
Increased small liana abundance in wider (W2 and
DISCUSSION W3)alteredriparianforests(Table1)isconsistentwith
Hotter and drier understories in altered compared to some previous studies in upland forest fragments
intact riparian forests, which produced conditions (Laurance et al. 2002, 2007), but the pattern did not
conducivetogreaterplantwaterlossfromleavesduring holdforthenarrow(W1)alteredriparianforestsorfor
thedryseason(Fig.2),wereconsistentwiththefindings larger((cid:2)5cmdbh)lianas.Williams-Linera(1990)found
of other studies that compared fragmented and intact increasedabundanceoflarge((cid:2)5cmdbh),butnotsmall
upland forests (Kapos 1989, Williams-Linera 1990, (,5 cm dbh) lianas near forest edges. In fragmented
Murcia 1995, Gascon et al. 2000, Laurance et al. forests (Laurance et al. 2002) and non-fragmented
2002). Altered microclimatic conditions at forest edges forests (Phillips et al. 2002), and among a variety of
can penetrate up to 100 m toward the forest interior forest systems (Oliveira et al. 2013), lianas have been
(Laurance et al. 2002). We found these differences correlated with higher tree mortality and changes in
permeated the entirety of the forest fragment (185–210 forest structure and species composition. We found no
m wide) in the dry season. Changes to microclimate of evidencethatgreaterabundanceofsmalllianasaffected
thismagnitudeareassociatedwithplantstressandhave forest structure by increasing tree mortality as found
been linked to higher tree mortality in other forest elsewhere (Lauranceetal. 1998, 2002).
fragments (Kapos 1989, Benitez-Malvido 1998, Laur- OriginalforestclearingatFazendaTangurooccurred
ance et al. 2002) in plants lacking drought-tolerant in the early 1980s and land was used for cattle pasture
characteristics. for ;20 years until conversion to soybean cultivation
Reduced abundances of seedlings and saplings in from2003to2008(Riskinetal.2013).Itispossiblethat
altered riparian fragments (Tables 1 and 2) were also changestoforeststructuretookplaceclosertothetime
consistent with findings in upland forest fragments of initial land clearing, but that over time these effects
(Benitez-Malvido 1998, Gascon et al. 2000, Santo-Silva have lessened as altered riparian forest edges fill in, as
et al. 2012). The mechanisms that caused reduced has occurred in some forest fragments (Didham and
seedlingandsaplingabundancearenotknown.Greater Lawton1999,Lauranceetal.2002;butseeLauranceet
reduction in seedling (edge locations only) and sapling al. 1998). This would cause microclimate differences to
(alllocations)abundancesinnarrow(W1)thanmedium lessen at forest edges. We found that LAI at riparian
(W2) and in medium than wide (W3) altered riparian forest edges was not significantly different between
zones may indicate a tolerance threshold (Question 3) altered and intact sites, but that microclimatic differ-
beyondwhichtheestablishmentofseedlingsorsurvival ences existed at forest edges, lending only partial
of saplings is reduced. Inhibited regeneration mayhave support to this idea. We did not have the long-term
consequences for the future of altered riparian zones, recruitment data and relative rates of recruitment vs.
but it remains to be seen if reductions in seedling and mortalityneededto furtherevaluatethis possibility.
saplingabundancewillpropagatetolargersizeclassesof Alternatively, there are several reasons why larger
trees. Because tree longevity in tropical forests is high, woodyplantsinalteredriparianforestsmaybebuffered
reduced seedling and sapling abundance suggests the against the changes to forest structure that often result
possibility of an extinction debt, or inevitable future fromfragmentation.A higherwater tablerelativetothe
extinctionscausedbypastevents(Magnagoetal.2013). groundsurfaceinalteredriparianforestscomparedwith
Thesizedistributionandnumberofallstandinglarge intact riparianforests (Fig. 3) mayalleviate some of the
woodyplants,deadlargewoodyplants,annualmortal- stressfromthehotter,drierconditionsandgreaterwater
ity, and biomass and C storage in altered and intact lossattheleaflevelexperiencedby plantsatforest–field
riparian forests were similar. The lack of significant edges(Question4).Insomelocations,maturetreesnear
differences in the structure of the large woody plant streamsuseprimarilydeepwater(DawsonandEhleringer
community 30 years after forest clearing contrasts with 1991),andinsomecases,accesstosoilwatercansustain
increases in tree mortality and reduced tree biomass plantproductivityunderconditionsofincreasedtemper-
associated with fragmentation and edge creation in aturesandlowerhumidity(LobellandGourdji2012).
upland areas (Kapos 1989, Williams-Linera 1990, It is also possible that microclimate changes on the
Lauranceetal.1998,2002).Itwasmoreconsistentwith orderofthosewemeasuredhavelittleornoinfluenceon
resultsfrom naturallyisolated galleryforests(Meaveet tree condition. Kapos (1989) found that in the rainy
al.1991,MacDougallandKellman1992,Kellmanetal. season,ahotteranddriermicroclimatenearforestedges
1998). Mean LAI was lower in altered riparian forests did not cause plant water deficits in understory shrubs
thanintactriparianforests,butthisresultwasdrivenby compared with interior forest shrubs, suggesting that
onelargeopenpatchalongonestream(alteredstream2; theseplantsreducedtheirstomatalconductanceandthus
Fig. 4). Thus, the pattern of more and larger gaps in controlled water loss despite microclimatic differences.